Long-term supplementation of honokiol and magnolol ameliorates body fat accumulation, insulin resistance, and adipose inflammation in high-fat fed mice

Molecular Nutrition and Food Research

Volumn 57, Issue 11, 2013, Pages 1988-1998

  Kim, Young Je ^a   Choi, Myung Sook ^a   Cha, Byung Yoon ^b   Woo, Je Tae ^c   Park, Yong Bok ^a   Kim, Sang Ryong ^a   Jung, Un Ju ^a  

^a Kyungpook National University   (South Korea)

^b CHUBU UNIVERSITY   (Japan)

^c Yuto Teruya Oknawa Research Center Co Ltd   (Japan)

Author keywords

Adipogenesis; Antiobesity; Honokiol; Inflammation; Magnolol

Indexed keywords

ADIPONECTIN; BIPHENYL DERIVATIVE; CCL2 PROTEIN, MOUSE; CHOLESTEROL; HONOKIOL; INTERLEUKIN 10; INTERLEUKIN 6; LIGNAN; MAGNOLOL; MONOCYTE CHEMOTACTIC PROTEIN 1; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA;

ADIPOGENESIS; ANIMAL; ANTIOBESITY; ARTICLE; BLOOD; BODY WEIGHT; C57BL MOUSE; DIET SUPPLEMENTATION; DRUG EFFECT; ENERGY METABOLISM; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN RESISTANCE; LIPID DIET; LIVER; MALE; METABOLISM; MOUSE; OBESITY; WHITE ADIPOSE TISSUE;

ADIPOGENESIS; ANTIOBESITY; HONOKIOL; INFLAMMATION; MAGNOLOL;

ADIPOGENESIS; ADIPONECTIN; ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; BIPHENYL COMPOUNDS; BLOOD GLUCOSE; BODY WEIGHT; CHEMOKINE CCL2; CHOLESTEROL; DIET, HIGH-FAT; DIETARY SUPPLEMENTS; ENERGY METABOLISM; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN RESISTANCE; INTERLEUKIN-10; INTERLEUKIN-6; LIGNANS; LIVER; MALE; MICE; MICE, INBRED C57BL; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84886791726     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201300113     Document Type: Article

References (59)

1. Rossner, S., Obesity: the disease of the twenty-first century. Int. J. Obes. 2002, 26, S2-S4.
2. Gallagher, E.-J., Leroith, D., Karnieli, E., Insulin resistance in obesity as the underlying cause for the metabolic syndrome. Mt. Sinai. J. Med. 2010, 77, 511-523.
3. Wellen, K.-E., Hotamisligil, G.-S., Inflammation, stress, and diabetes. J. Clin. Invest. 2005, 5, 1111-1119.
4. Jo, J., Gavrilova, O., Pack, S., Jou, W. et al., Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput. Biol. 2009, 5, e1000324.
5. Antuna-Puente, B., Feve, B., Fellahi, S., Bastard, J.-P., Adipokines: the missing link between insulin resistance and obesity. Diabetes Metab. 2008, 34, 2-11.
6. Steppan, C.-M., Bailey, S.-T., Bhat, S., Brown, E.-J. et al., The hormone resistin links obesity to diabetes. Nature 2001, 409, 307-312.
7. Chiang, S.-H., Bazuine, M., Lumeng, C.-N., Geletka, L.-M. et al., The protein kinase IKKepsilon regulates energy balance in obese mice. Cell 2009, 138, 961-975.
8. Weyer, C., Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J. Clin. Endocrinol. Metab. 2001, 86, 1930-1935.
9. van Exel, E., Gussekloo, J., de Craen, A.-J., Frölich, M. et al., Low production capacity of interleukin-10 associates with the metabolic syndrome and type 2 diabetes: the Leiden 85-Plus Study. Diabetes 2002, 51, 1088-1092.
10. Calder, P.-C., Ahluwalia, N., Brouns, F., Buetler, T., Dietary factors and low-grade inflammation in relation to overweight and obesity. Br. J. Nutr. 2011, 106, S5-S78.
11. Heidemann, C., Scheidt-Nave, C., Richter, A., Mensink, G.-B., Dietary patterns are associated with cardiometabolic risk factors in a representative study population of German adults. Br. J. Nutr. 2011, 106, 1253-1262.
12. Mors, W.-B., Rizzini, C.-T., Pereira, N.-A. (Eds.), Medicinal Plants of Brazil. Reference Publication, Inc., Michigan, 2002.
13. Tomas, S. C.-Li. (Ed.), Chinese and Related North American Herbs: Phytopharmacology and Therapeutic Values. CRC Press, Boca Raton, FL 2002.
14. Maruyama, Y., Kuribara, H., Overview of the pharmacological features of honokiol. CNS Drug. Rev. 2000, 6, 35-44.
15. Lee, J., Jung, E., Park, J., Jung, K., Anti-inflammatory effects of magnolol and honokiol are mediated through inhibition of the downstream pathway of MEKK-1 in NF-kappaB activation signaling. Planta. Med. 2005, 71, 338-343.
16. Sohn, E.-J., Kim, C.-S., Kim, Y.-S., Jung, D.-H., Effects of magnolol (5, 5_-diallyl-2, 2_-dihydroxybiphenyl) on diabetic nephropathy in type 2 diabetic Goto-Kakizaki rats. Life Sci. 2007, 80, 468-475.
17. Choi, S.-S., Cha, B.-Y., Lee, Y.-S., Yonezawa, T. et al., Magnolol enhances adipocyte differentiation and glucose uptake in 3T3-L1 cells. Life Sci. 2009, 84, 908-914.
18. Choi, S.-S., Cha, B.-Y., Iida, K., Sato, M. et al., Honokiol enhances adipocyte differentiation by potentiating insulin signaling in 3T3-L1 preadipocytes. J. Nat. Med. 2011, 65, 424-430.
19. Yin, H.-Q., Kim, Y.-C., Chung, Y.-S., Kim, Y.-C. et al., Honokiol reverses alcoholic fatty liver by inhibiting the maturation of sterol regulatory element binding protein-1c and the expression of its downstream lipogenesis genes. Toxicol. Appl. Pharmacol. 2009, 236, 124-130.
20. Murakami, Y., Kawata, A., Seki, Y., Koh, T. et al., Comparative inhibitory effects of magnolol, honokiol, eugenol and bis-eugenol on cyclooxygenase-2 expression and nuclear factor-kappa b activation in RAW264.7 macrophage-like cells stimulated with fimbriae of Porphyromonas gingivalis. In Vivo 2012, 26, 941-950.
21. Collins, S., Martin, T.-L., Surwit, R.-S., Robidoux, J., Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 2004, 81, 243-248.
22. Choi, S.-S., Cha, B.-Y., Iida, K., Sato, M. et al., Honokiol enhances adipocyte differentiation by potentiating insulin signaling in 3T3-L1 preadipocytes. J. Nat. Med. 2011, 65, 424-430.
23. Folch, J., Lees, M., Sloan-Stanley, G. H., A simple method for isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226, 497-509.
24. Kim, H.-J., Lee, K.-T., Park, Y.-B., Jeon, S.-M. et al., Dietary docosahexaenoic acid-rich diacylglycerols ameliorate hepatic steatosis and alter hepatic gene expressions in C57BL/6J-Lep(ob/ob) mice. Mol. Nutr. Food Res. 2008, 52, 965-973.
25. Carl, M.-N., Lakshmanan, M.-R., Porter, J.-W., Fatty acid synthase from rat liver. Meth. Enzymol. 1975, 35, 37-44.
26. Markwell M, A.-K., McGroarty, E.-J., Bieber, L.-L., Tolbert, N.-E., The subcellular distribution of carnitine acyltransferases in mammalian liver and kidney. J. Biol. Chem. 1973, 248, 3426-3432.
27. Lazarow, P.-B., Assay of peroxisomal β-oxidation of fatty acids. Meth. Enzymol. 1981, 72, 315-319.
28. Bradford, M.-M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
29. Schmittgen, T.-D., Livak, K.-J., Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3, 1101-1108.
30. Moller, D.-E., Flier, J., Insulin resistance-mechanism, syndromes, and implications. N. Engl. J. Med. 1991, 325, 938-948.
31. Anderson, R. A., Chromium and polyphenols from cinnamon improve insulin sensitivity. Proc. Nutr. Soc. 2008, 67, 48-53.
32. Sacco, S. M., Horcajada, M. N., Offord, E., Phytonutrients for bone health during ageing. Br. J. Clin. Pharmacol. 2013, 75, 697-707.
33. Kim, J.-B., Spiegelman, B.-M., ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev. 1996, 10, 1096-1107.
34. Sampath, H., Miyazaki, M., Dobrzyn, A., Ntambi, J.-M., Stearoyl-CoA desaturase-1 mediates the pro-lipogenic effects of dietary saturated fat. J. Biol. Chem. 2007, 282, 2483-2493.
35. Lodhi, I.-J., Yin, L., Jensen-Urstad, A.-P., Funai, K. et al., Inhibiting adipose tissue lipogenesis reprograms thermogenesis and PPAR-γ activation to decrease diet-induced obesity. Cell Metab. 2012, 16, 189-201.
36. Ntambi, J.-M., Miyazaki, M., Stoehr, J.-P., Lan, H. et al., Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. USA 2002, 99, 11482-11486.
37. Hajri, T., Hall, A.-M., Jensen, D.-R., Pietka, T.-A. et al., CD36-facilitated fatty acid uptake inhibits leptin production and signaling in adipose tissue. Diabetes 2007, 56, 1872-1880.
38. Priego, T., Sánchez, J., Palou, A., Picó, C., Leptin intake during the suckling period improves the metabolic response of adipose tissue to a high-fat diet. Int. J. Obes. 2010, 34, 809-819.
39. Smith, U., Gogg, S., Johansson, A., Olausson, T. et al., Thiazolidinediones (PPARgamma agonists) but not PPARalpha agonists increase IRS-2 gene expression in 3T3-L1 and human adipocytes. Faseb. J. 2001, 15, 215-220.
40. Miki, H., Yamauchi, T., Suzuki, R., Komeda, K. et al., Essential role of insulin receptor substrate 1 (IRS-1) and IRS-2 in adipocyte differentiation. Mol. Cell. Biol. 2001, 21, 2521-2532.
41. Yao-Borengasser, A., Rassouli, N., Varma, V., Bodles, A.-M. et al., Stearoyl-coenzyme A desaturase 1 gene expression increases after pioglitazone treatment and is associated with peroxisomal proliferator-activated receptor-gamma responsiveness. J. Clin. Endocrinol. Metab. 2008, 93, 4431-4439.
42. Choi, S.-S., Cha, B.-Y., Lee, Y.-S., Yonezawa, T. et al., Magnolol enhances adipocyte differentiation and glucose uptake in 3T3-L1 cells. Life Sci. 2009, 84, 908-914.
43. Alonso-Castro, A.J., Zapata-Bustos, R., Domínguez, F., García-Carrancá, A. et al., Magnolia dealbata Zucc and its active principles honokiol and magnolol stimulate glucose uptake in murine and human adipocytes using the insulin-signaling pathway. Phytomedicine 2011, 18, 926-933.
44. Choi, S.-S., Cha, B.-Y., Iida, K., Sato, M. et al., Honokiol enhances adipocyte differentiation by potentiating insulin signaling in 3T3-L1 preadipocytes. J. Nat. Med. 2011, 65, 424-430.
45. Jiang, G., Dallas-Yang, Q., Li, Z., Szalkowski, D. et al., Potentiation of insulin signaling in tissues of Zucker obese rats after acute and long-term treatment with PPARgamma agonists. Diabetes 2002, 51, 2412-2419.
46. Rieusset, J., Touri, F., Michalik, L., Escher, P. et al., A new selective peroxisome proliferator-activated receptor gamma antagonist with antiobesity and antidiabetic activity. Mol. Endocrinol. 2002, 16, 2628-2644.
47. Wueest, S., Rapold, R.-A., Schumann, D.-M., Rytka, J.-M. et al., Deletion of Fas in adipocytes relieves adipose tissue inflammation and hepatic manifestations of obesity in mice. J. Clin. Invest. 2010, 120, 191-202.
48. Perdomo, G., Commerford, S.-R., Richard, A.-M., Adams, S.-H. et al., Increased beta-oxidation in muscle cells enhances insulin-stimulated glucose metabolism and protects against fatty acid-induced insulin resistance despite intramyocellular lipid accumulation. J. Biol. Chem. 2004, 279, 27177-27186.
49. Banerjee, R.-R., Rangwala, S.-M., Shapiro, J.-S., Rich, A.-S. et al., Regulation of fasted blood glucose by resistin. Science 2004, 303, 1195-1198.
50. Maeda, N., Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 2002, 8, 731-737.
51. Yamauchi, T., Kamon, J., Minokoshi, Y., Ito, Y. et al., Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat. Med. 2002, 8, 1288-1295.
52. Lau, C.-H., Muniandy, S., Novel adiponectin-resistin (AR) and insulin resistance (IRAR) indexes are useful integrated diagnostic biomarkers for insulin resistance, type 2 diabetes and metabolic syndrome: a case control study. Cardiovasc. Diabetol. 2011, 10, 1-8.
53. Cho, S., Choi, Y., Park, S., Park, T., Carvacrol prevents diet-induced obesity by modulating gene expressions involved in adipogenesis and inflammation in mice fed with high-fat diet. J. Nutri. Biochem. 2011, 23, 192-201.
54. Medzhitov, R., Toll-like receptors and innate immunity. Nat. Rev. Immunol. 2001, 1, 135-145.
55. Shi, H., Kokoeva, M.-V., Inouye, K., Tzameli, I. et al., TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 2006, 116, 3015-3025.
56. Davis, J.-E., Braucher, D.-R., Walker-Daniels, J., Spurlock, M.-E., Absence of TLR2 protects against high-fat diet-induced inflammation and results in greater insulin-stimulated glucose transport in cultured adipocytes. J. Nutr. Biochem. 2011, 22, 136-141.
57. Pamir, N., McMillen, T.-S., Edgel, K.-A., Kim, F. et al., Deficiency of lymphotoxin-α does not exacerbate high-fat diet-induced obesity but does enhance inflammation in mice. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E961-E971.
58. Lumeng, C.-N., Bodzin, J.-L., Saltiel, A.-R., Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 2007, 117, 175-184.
59. Ouyang, W., Rutz, S., Crellin, N.-K., Valdez, P.-A. et al., Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu. Rev. Immunol. 2011, 29, 71-109.